Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-22T12:02:06.311Z Has data issue: false hasContentIssue false
  • English
  • Français

Generalizability and comparability of prevalence estimates in the wild bird literature: methodological and epidemiological considerations

Published online by Cambridge University Press:  18 February 2020

Nadine A. Vogt Open the ORCID record for Nadine A. Vogt [Opens in a new window] ,
Christian P.G. Stevens ,
David L. Pearl ,
Eduardo N. Taboada  and
Claire M. Jardine
Nadine A. Vogt*
Affiliation:
Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada
Christian P.G. Stevens
Affiliation:
Department of Philosophy, King's College London, Strand, London, England
David L. Pearl
Affiliation:
Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada
Eduardo N. Taboada
Affiliation:
National Microbiology Laboratory, Public Health Agency of Canada, Lethbridge, Alberta, Canada
Claire M. Jardine
Affiliation:
Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada
*
Author for correspondence: Nadine A. Vogt, Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Wild birds have been the focus of a great deal of research investigating the epidemiology of zoonotic bacteria and antimicrobial resistance in the environment. While enteric pathogens (e.g. Campylobacter, Salmonella, and E. coli O157:H7) and antimicrobial resistant bacteria of public health importance have been isolated from a wide variety of wild bird species, there is a considerable variation in the measured prevalence of a given microorganism from different studies. This variation may often reflect differences in certain ecological and biological factors such as feeding habits and immune status. Variation in prevalence estimates may also reflect differences in sample collection and processing methods, along with a host of epidemiological inputs related to overall study design. Because the generalizability and comparability of prevalence estimates in the wild bird literature are constrained by their methodological and epidemiological underpinnings, understanding them is crucial to the accurate interpretation of prevalence estimates. The main purpose of this review is to examine methodological and epidemiological inputs to prevalence estimates in the wild bird literature that have a major bearing on their generalizability and comparability. The inputs examined here include sample type, microbiological methods, study design, bias, sample size, definitions of prevalence outcomes and parameters, and control of clustering. The issues raised in this review suggest, among other things, that future prevalence studies of wild birds should avoid opportunistic sampling when possible, as this places significant limitations on the generalizability of prevalence data.

Keywords

Epidemiologystudy designwildlifezoonoses
Type
Review Article
Information
Animal Health Research Reviews , Volume 21 , Issue 1 , June 2020 , pp. 89 - 95
Check for updates
Copyright
Copyright © Cambridge University Press 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allen, SE, Janecko, N, Pearl, DL, Boerlin, P, Reid-Smith, RJ and Jardine, CM (2013) Comparison of Escherichia coli recovery and antimicrobial resistance in cecal, colon, and fecal samples collected from wild house mice (Mus Musculus). Journal of Wildlife Diseases 49, 432–436.CrossRefGoogle Scholar
Anderson, DR (2001) The need to get the basics right in wildlife field studies. Wildlife Society Bulletin 29, 1294–1297.Google Scholar
Anjum, MF, Zankari, E and Hasman, H (2017) Molecular methods for detection of antimicrobial resistance. Microbiology Spectrum 5.Google ScholarPubMed
Benskin, CM, Wilson, K, Jones, K and Hartley, IR (2009) Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biological Reviews 84, 349–373.CrossRefGoogle ScholarPubMed
Bowler, DE, Nilsen, EB, Bischof, R, O'Hara, RB, Yu, TT, Oo, T, Aung, M and Linnell, JDC (2019) Integrating data from different survey types for population monitoring of an endangered species: the case of the Eld's deer. Scientific Reports 9, 7766.CrossRefGoogle ScholarPubMed
Broman, T, Palmgren, H, Bergstrom, S, Sellin, M, Waldenström, J, Danielsson-Tham, ML and Olsen, B (2002) Campylobacter jejuni in black-headed gulls (Larus ridibundus): prevalence, genotypes, and influence on C. jejuni epidemiology. Journal of Clinical Microbiology 40, 4594–4602.CrossRefGoogle ScholarPubMed
Carroll, D, Wang, J, Fanning, S and Mcmahon, BJ (2015) Antimicrobial resistance in wildlife: implications for public health. Zoonoses and Public Health 62, 534–542.CrossRefGoogle ScholarPubMed
Cole, D, Drum, DJV, Stallknecht, DE, White, DG, Lee, MD, Ayers, S, Sobsey, M and Maurer, JJ (2005) Free-living Canada geese and antimicrobial resistance. Emerging Infectious Diseases 11, 935–938.CrossRefGoogle ScholarPubMed
Colles, FM, McCarthy, ND, Howe, JC, Devereux, CL, Gosler, AG and Maiden, MCJ (2009) Dynamics of Campylobacter colonization of a natural host, Sturnus vulgaris (European Starling). Environmental Microbiology 11, 258–267.CrossRefGoogle Scholar
Conn, PB, Thorson, JT and Johnson, DS (2017) Confronting preferential sampling when analysing population distributions: diagnosis and model-based triage. Methods in Ecology and Evolution 8, 1535–1546.CrossRefGoogle Scholar
Dohoo, I, Martin, W and Stryhn, H (2014) Veterinary Epidemiologic Research, 3rd Edn. Charlottetown, Prince Edward Island: VER Inc..Google Scholar
Ferens, WA and Hovde, CJ (2011) Escherichia coli O157:H7: animal reservoir and sources of human infection. Foodborne Pathogens and Disease 8, 465–487.CrossRefGoogle ScholarPubMed
Girdwood, RW, Fricker, CR, Munro, D, Shedden, CB and Monaghan, P (1985) The incidence and significance of Salmonella carriage by gulls (Larus spp.) in Scotland. Journal of Hygiene 95, 229–241.CrossRefGoogle Scholar
Guenther, S, Grobbel, M, Lübke-Becker, A, Goedecke, A, Friedrich, ND, Wieler, LH and Ewers, C (2010) Antimicrobial resistance profiles of Escherichia coli from common European wild bird species. Veterinary Microbiology 144, 219–225.CrossRefGoogle ScholarPubMed
Hald, B, Skov, MN, Nielsen, EM, Rahbek, C, Madsen, JJ, Wainø, M, Chriél, M, Nordentoft, S, Baggesen, DL and Madsen, M (2016) Campylobacter jejuni and Campylobacter coli in wild birds on Danish livestock farms. Acta Veterinaria Scandinavica 58, 11.CrossRefGoogle ScholarPubMed
Hayek, L-A and Buzas, MA (1997) Surveying Natural Populations. New York, USA: Columbia University.Google Scholar
Hazra, A (2017) Using the confidence interval confidently. Journal of Thoracic Disease 9, 4125–4130.CrossRefGoogle ScholarPubMed
Hombach, M, Bloemberg, GV and Böttger, EC (2012) Effects of clinical breakpoint changes in CLSI guidelines 2010/2011 and EUCAST guidelines 2011 on antibiotic susceptibility test reporting of Gram-negative bacilli. Journal of Antimicrobial Chemotherapy 67, 622–632.CrossRefGoogle ScholarPubMed
Hughes, LA, Bennett, M, Coffey, P, Elliott, J, Jones, TR, Jones, RC, Lahuerta-Marin, A, McNiffe, K, Norman, D, Williams, NJ and Chantry, J (2009) Risk factors for the occurrence of Escherichia coli virulence genes eae, stx1 and stx2 in wild bird populations. Epidemiology and Infection 137, 1574–1582.CrossRefGoogle ScholarPubMed
Ito, K, Kubokura, Y, Kaneko, KI, Totake, Y and Ogawa, M (1988) Occurrence of Campylobacter jejuni in free-living wild birds from Japan. Journal of Wildlife Diseases 24, 467–470.CrossRefGoogle ScholarPubMed
Jiménez Gómez, PA, García De Los Ríos, JE, Mendoza, AR, De, P, Ramonet, P, Albiach, RG and Reche Sainz, MP (2004) Molecular basis of quinolone resistance in Escherichia coli from wild birds. The Canadian Journal of Veterinary Research 68, 229–231.Google ScholarPubMed
Jorgensen, JH and Ferraro, MJ (2009) Antimicrobial susceptibility testing: a review of general principles and contemporary practices. Clinical Infectious Diseases 49, 1749–1755.CrossRefGoogle ScholarPubMed
Jourdain, E, Gauthier-Clerc, M, Bicout, D and Sabatier, P (2007) Bird migration routes and risk for pathogen dispersion into western Mediterranean wetlands. Emerging Infectious Diseases 13, 365–372.CrossRefGoogle ScholarPubMed
Jurado-Tarifa, E, Torralbo, A, Borge, C, Cerdà-Cuéllar, M, Ayats, T, Carbonero, A and García-Bocanegra, I (2016) Genetic diversity and antimicrobial resistance of Campylobacter and Salmonella strains isolated from decoys and raptors. Comparative Immunology, Microbiology and Infectious Diseases 48, 14–21.CrossRefGoogle ScholarPubMed
Kapperud, G and Rosef, O (1983) Avian wildlife reservoir of Campylobacter fetus subsp. jejuni, Yersinia spp. and Salmonella spp. in Norway. Applied Environmental Microbiology 45, 375–380.CrossRefGoogle ScholarPubMed
Kelly, TR and Sleeman, JM (2003) Morbidity and mortality of red foxes (Vulpes vulpes) and gray foxes (Urocyon cinereoargenteus) admitted to the wildlife center of Virginia, 1993–2001. Journal of Wildlife Diseases 39, 467–469.CrossRefGoogle Scholar
Kirk, JH, Holmberg, CA and Jeffrey, JS (2002) Prevalence of Salmonella spp. in selected birds captured on California dairies. Journal of the American Veterinary Medical Association 220, 359–362.CrossRefGoogle ScholarPubMed
LeJeune, JT and Pearl, DL (2014) Wildlife and Environmental Contributions to the Contamination of Meats with Antimicrobial-Resistant bacteria, in Encyclopedia of meat sciences, 2nd Edn. San Diego, United States: Academic Press Inc.Google Scholar
Liakopoulos, A, Mevius, DJ, Olsen, B and Bonnedahl, J (2016) The colistin resistance mcr-1 gene is going wild. Journal of Antimicrobial Chemotherapy 71, 2335–2336.CrossRefGoogle ScholarPubMed
Love, BC and Rostagno, MH (2008) Comparison of five culture methods for Salmonella isolation from swine fecal samples of known infection status. Journal of Veterinary Diagnostic Investigation 20, 620–624.CrossRefGoogle ScholarPubMed
Luechtefeld, NA, Blaser, MJ, Reller, LB and Wang, WL (1980) Isolation of Campylobacter fetus subsp. jejuni from migratory waterfowl. Journal of Clinical Microbiology 12, 406–408.CrossRefGoogle ScholarPubMed
MacKinnon, MC, Pearl, DL, Carson, CA, Parmley, EJ and McEwen, SA (2018) Comparison of annual and regional variation in multidrug resistance using various classification metrics for generic Escherichia coli isolated from chicken abattoir surveillance samples in Canada. Preventive Veterinary Medicine 154, 9–17.CrossRefGoogle ScholarPubMed
Magiorakos, AP, Srinivasan, A, Carey, RB, Carmeli, Y, Falagas, ME, Giske, CG, Harbarth, S, Hindler, JF, Kahlmeter, G, Olsson-Liljequist, B, Paterson, DL, Rice, LB, Stelling, J, Struelens, MJ, Vatopoulos, A, Weber, JT and Monnet, DL (2012) Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection 18, 268–281.CrossRefGoogle ScholarPubMed
Martin, SW (1984) Estimating disease prevalence and the interpretation of screening test results. Preventive Veterinary Medicine 2, 463–472.CrossRefGoogle Scholar
McGarigal, K, Cushman, SA and Stafford, S (2000) Multivariate Statistics for Wildlife and Ecology Research. Berlin, Germany: Springer.CrossRefGoogle Scholar
Medalla, F, Hoekstra, RM, Whichard, JM, Barzilay, EJ, Chiller, TM, Joyce, K, Rickert, R, Krueger, A, Stuart, A and Griffin, PM (2013) Increase in resistance to ceftriaxone and nonsusceptibility to ciprofloxacin and decrease in multidrug resistance among Salmonella strains, United States, 1996–2009. Foodborne Pathogens and Disease 10, 302–309.CrossRefGoogle ScholarPubMed
Michelangeli, M, Wong, BBM and Chapple, DG (2015) It's a trap: sampling bias due to animal personality is not always inevitable. Behavioural Ecology 27, 62–67.CrossRefGoogle Scholar
Mi'kanatha, NM, Dettinger, LA, Perry, A, Rogers, P, Reynolds, SM and Nachamkin, I (2012) Culturing stool specimens for Campylobacter spp., Pennsylvania, USA. Emerging Infectious Diseases 18, 484–487.CrossRefGoogle Scholar
Morabito, S, Dell'Omo, G, Agrimi, U, Schmidt, H, Karch, H, Cheasty, T and Caprioli, A (2001) Detection and characterization of Shiga toxin-producing Escherichia coli in feral pigeons. Veterinary Microbiology 82, 275–283.CrossRefGoogle ScholarPubMed
Moré, E, Ayats, T, Ryan, PG, Naicker, PR, Keddy, KH, Gaglio, D, Witteveen, M and Cerdà-Cuéllar, M (2017) Seabirds (Laridae) as a source of Campylobacter spp., Salmonella spp. and antimicrobial resistance in South Africa. Environmental Microbiology 19, 4164–4176.CrossRefGoogle ScholarPubMed
Morishita, TY, Aye, PP, Ley, EC and Harr, BS (1999) Survey of pathogens and blood parasites in free-living passerines. Avian Diseases 43, 549–552.CrossRefGoogle ScholarPubMed
Nusser, SM, Clark, WR, Otis, DL and Huang, L (2008) Sampling considerations for disease surveillance in wildlife populations. Journal of Wildlife Management 72, 52–60.CrossRefGoogle Scholar
Pinto, A, Simõ, R, Oliveira, M, Vaz-Pires, P, Brandã, R and Martins Da Costa, P (2015) Multidrug resistance in wild bird populations: importance of the food chain. Journal of Zoo and Wildlife Medicine 46, 723–731.CrossRefGoogle ScholarPubMed
Priyanka, B, Patil, RK and Dwarakanath, S (2016) A review on detection methods used for foodborne pathogens. The Indian Journal of Medical Research 144, 327–338.CrossRefGoogle ScholarPubMed
Radhouani, H, Poeta, P, Goncalves, A, Pacheco, R, Sargo, R and Igrejas, G (2012) Wild birds as biological indicators of environmental pollution: antimicrobial resistance patterns of Escherichia coli and enterococci isolated from common buzzards (Buteo Buteo). Journal of Medical Microbiology 61, 837–843.CrossRefGoogle Scholar
Reboredo-Fernández, A, Ares-Mazás, E, Cacciò, SM and Gómez-Couso, H (2015) Occurrence of Giardia and Cryptosporidium in wild birds in Galicia (Northwest Spain). Parasitology 142, 917–925.CrossRefGoogle Scholar
Reed, KD, Meece, JK, Henkel, JS and Shukla, SK (2003) Birds, migration and emerging zoonoses: West Nile virus, Lyme disease, Influenza A and enteropathogens. Clinical Medicine and Research 1, 5–12.CrossRefGoogle ScholarPubMed
Rodgers, JD, Simpkin, E, Lee, R, Clifton-Hadley, FA and Vidal, AB (2017) Sensitivity of direct culture, enrichment and PCR for detection of Campylobacter jejuni and C. coli in broiler flocks at slaughter. Zoonoses and Public Health 64, 262–271.CrossRefGoogle Scholar
Silva, N, Igrejas, G, Rodrigues, P, Rodrigues, T, Goncalves, A, Felgar, AC, Pacheco, R, Gonçalves, D, Cunha, R and Poeta, P (2011) Molecular characterization of vancomycin-resistant enterococci and extended-spectrum beta-lactamase-containing Escherichia coli isolates in wild birds from the Azores Archipelago. Avian Pathology 40, 473–479.CrossRefGoogle ScholarPubMed
Shobrak, MY and Abo-Amer, AE (2014) Role of wild birds as carriers of multi-drug resistant Escherichia coli and Escherichia vulneris. Brazilian Journal of Microbiology 45, 1199–1209.CrossRefGoogle ScholarPubMed
Skov, MN, Madsen, JJ, Rahbek, C, Lodal, J, Jespersen, JB, Jørgensen, JC, Dietz, HH, Chriél, M and Baggesen, DL (2008) Transmission of Salmonella between wildlife and meat-production animals in Denmark. Journal of Applied Microbiology 105, 1558–1568.CrossRefGoogle ScholarPubMed
Spalding, MG and Forrester, DJ (1993) Disease monitoring of free-ranging and released wildlife. Journal of Zoo and Wildlife Medicine 24, 271–280.Google Scholar
Steidl, RJ, Hayes, JP and Schauber, E (1997) Statistical power analysis in wildlife research. The Journal of Wildlife Management 61, 270–279.CrossRefGoogle Scholar
Thapaliya, D, Dalman, M, Kadariya, J, Little, K, Mansell, V, Taha, MY, Grenier, D and Smith, TC (2017) Characterization of Staphylococcus aureus in goose feces from state parks in northeast Ohio. EcoHealth 14, 303–309.CrossRefGoogle ScholarPubMed
Vidal, A, Baldomà, L, Molina-López, RA, Martin, M and Darwich, L (2017) Microbiological diagnosis and antimicrobial sensitivity profiles in diseased free-living raptors. Avian Pathology 46, 442–450.CrossRefGoogle ScholarPubMed
Videvall, E, Strandh, M, Engelbrecht, A, Cloete, S and Cornwallis, CK (2018) Measuring the gut microbiome in birds: comparison of faecal and cloacal sampling. Molecular Ecology Resources 18, 424–434.CrossRefGoogle ScholarPubMed
Vittecoq, M, Laurens, C, Brazier, L, Durand, P, Elguero, E, Arnal, A, Thomas, F, Aberkane, S, Renaud, N, Prugnolle, F, Solassol, J, Jean-Pierre, H, Godreuil, S and Renaud, F (2017) VIM-1 carbapenemase-producing Escherichia coli in gulls from southern France. Ecology and Evolution 7, 1224–1232.CrossRefGoogle ScholarPubMed
Vogt, NA, Pearl, DL, Taboada, EN, Mutschall, SK, Janecko, N, Reid-Smith, R, Bloomfield, B and Jardine, CM (2018) Epidemiology of Campylobacter. Salmonella, and antimicrobial resistant E. coli in free-living Canada geese (Branta canadensis) from three sources in southern Ontario. Zoonoses and Public Health 65, 873–886.CrossRefGoogle ScholarPubMed
Vogt, NA, Pearl, DL, Taboada, EN, Reid-Smith, RJ, Mulvey, MR, Janecko, N, Mutchall, SK and Jardine, CM (2019) A repeated cross-sectional study of the epidemiology of Campylobacter and antimicrobial resistant Enterobacteriaceae in free-living Canada geese in Guelph, Ontario, Canada. Zoonoses and Public Health 66, 60–72.CrossRefGoogle ScholarPubMed
Waldenström, J, On, SLW, Ottvall, R, Hasselquist, D and Olsen, B (2007) Species diversity of campylobacteria in a wild bird community in Sweden. Journal of Applied Microbiology 102, 1–9.CrossRefGoogle Scholar
Wallace, JS, Cheasty, T and Jones, K (1997) Isolation of Vero cytotoxin-producing Escherichia coli O157 from wild birds. Journal of Applied Microbiology 82, 399–404.CrossRefGoogle ScholarPubMed
Wang, J, Ma, ZB, Zeng, ZL, Yang, XW, Huang, Y and Liu, JH (2017) The role of wildlife (wild birds) in the global transmission of antimicrobial resistance genes. Zoological Research 38, 55–80.Google ScholarPubMed
Wobeser, GA (2007) Disease in Wild Animals: Investigation and Management, 2nd Edn. New York: Springer.CrossRefGoogle Scholar
World Health Organization (2017) WHO list of Critically Important Antimicrobials for Human Medicine (WHO CIA List). Geneva, Switzerland: Advisory group on integrated surveillance of antimicrobial resistance (AGISAR). Available at http://www.who.int/foodsafety/publications/cia2017.pdf?ua=1Google Scholar